Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow

Understanding patterns of connectivity among populations of marine organisms is essential for the development of realistic, spatially explicit models of population dynamics. Two approaches, empirical genetic patterns and oceanographic dispersal modelling, have been used to estimate levels of evolutionary connectivity among marine populations but rarely have their potentially complementary insights been combined. Here, a spatially realistic Lagrangian model of larval dispersal and a theoretical genetic model are integrated with the most extensive study of gene flow in a Caribbean marine organism. The 871 genets collected from 26 sites spread over the wider Caribbean subsampled 45.8% of the 1900 potential unique genets in the model. At a coarse scale, significant consensus between modelled estimates of genetic structure and empirical genetic data for populations of the reef‐building coral Montastraea annularis is observed. However, modelled and empirical data differ in their estimates of connectivity among northern Mesoamerican reefs indicating that processes other than dispersal may dominate here. Further, the geographic location and porosity of the previously described east–west barrier to gene flow in the Caribbean is refined. A multi‐prong approach, integrating genetic data and spatially realistic models of larval dispersal and genetic projection, provides complementary insights into the processes underpinning population connectivity in marine invertebrates on evolutionary timescales.

[1]  S. Andréfouët,et al.  Physical connectivity in the Mesoamerican Barrier Reef System inferred from 9 years of ocean color observations , 2009, Coral Reefs.

[2]  Patrick N. Halpin,et al.  Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation , 2007, Landscape Ecology.

[3]  K. R. Clarke,et al.  A taxonomic distinctness index and its statistical properties , 1998 .

[4]  M. Nei Analysis of gene diversity in subdivided populations. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[6]  Nathaniel Valière gimlet: a computer program for analysing genetic individual identification data , 2002 .

[7]  B. Kendall,et al.  The stochastic nature of larval connectivity among nearshore marine populations , 2008, Proceedings of the National Academy of Sciences.

[8]  GEOGRAPHIC DIFFERENCES IN SPECIES BOUNDARIES AMONG MEMBERS OF THE MONTASTRAEA ANNULARIS COMPLEX BASED ON MOLECULAR AND MORPHOLOGICAL MARKERS , 2004, Evolution; international journal of organic evolution.

[9]  H. Lessios,et al.  Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra , 2000, Molecular ecology.

[10]  Claire B Paris-Limouzy,et al.  Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs , 2009, Coral Reefs.

[11]  R. Bleck,et al.  Global Ocean Prediction with the Hybrid Coordinate Ocean Model , 2009 .

[12]  R. Warwick,et al.  The application of an indicator based on taxonomic distinctness for UK marine biodiversity assessments. , 2006, Journal of environmental management.

[13]  M. Slatkin Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations , 2004, Molecular ecology.

[14]  J. Pritchard,et al.  Documentation for structure software : Version 2 . 3 , 2009 .

[15]  W. J. Walsh,et al.  Phylogeography, historical demography, and the role of post-settlement ecology in two Hawaiian damselfish species , 2008 .

[16]  Claire B Paris-Limouzy,et al.  River-reef connectivity in the Meso-American Region , 2008, Coral Reefs.

[17]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[18]  Nicola L. Foster,et al.  Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. , 2007, The Journal of animal ecology.

[19]  M. Hellberg Gene Flow and Isolation among Populations of Marine Animals , 2009 .

[20]  Eric P. Chassignet,et al.  Ocean weather forecasting : an integrated view of oceanography , 2006 .

[21]  M. Hellberg,et al.  GEOGRAPHIC VARIATION IN CLONAL STRUCTURE IN A REEF- BUILDING CARIBBEAN CORAL, ACROPORA PALMATA , 2006 .

[22]  K. I. Ugland,et al.  The species–accumulation curve and estimation of species richness , 2003 .

[23]  E. Severance,et al.  Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals , 2006 .

[24]  K. R. Clarke,et al.  On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages , 2006 .

[25]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[26]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[27]  M. Stanhope,et al.  Genetic connectivity in the Florida reef system: comparative phylogeography of commensal invertebrates with contrasting reproductive strategies , 2006, Molecular ecology.

[28]  Peter J. Edmunds,et al.  The demographics of a 15-year decline in cover of the caribbean reef coral Montastraea annularis , 2007 .

[29]  E. McCoy,et al.  Long-distance dispersal and the reef-building corals of the Eastern Pacific , 1978 .

[30]  Johnathan T. Kool,et al.  An object-oriented, individual-based approach for simulating the dynamics of genes in subdivided populations , 2009, Ecol. Informatics.

[31]  Johnathan T. Kool,et al.  Complex migration and the development of genetic structure in subdivided populations: an example from Caribbean coral reef ecosystems , 2010 .

[32]  M. Miller,et al.  Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean , 2010, Coral Reefs.

[33]  Mark Spalding,et al.  World atlas of coral reefs , 2001 .

[34]  J. Woodley,et al.  Timing of reproduction in Montastraea annularis: relationship to environmental variables , 2002 .

[35]  J. Benzie Genetic structure of coral reef organisms: Ghosts of dispersal past , 1999 .

[36]  F. Muller‐Karger,et al.  Pigment distribution in the Caribbean sea: Observations from space , 1989 .

[37]  S. Palumbi,et al.  Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences , 2002, Molecular ecology.

[38]  D. Olson,et al.  Seascape Genetics: A Coupled Oceanographic-Genetic Model Predicts Population Structure of Caribbean Corals , 2006, Current Biology.

[39]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[40]  M. Hellberg,et al.  Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata , 2005, Molecular ecology.

[41]  K. R. Clarke,et al.  Taxonomic distinctness as a measure of diversity applied over a large scale: the benthos of the Norwegian continental shelf , 2005 .

[42]  E. Severance,et al.  Microsatellite loci isolated from the Caribbean coral, Montastraea annularis , 2004 .

[43]  Michael S. Taylor,et al.  Comparative phylogeography in a genus of coral reef fishes: biogeographic and genetic concordance in the Caribbean , 2006, Molecular ecology.

[44]  Claire B Paris-Limouzy,et al.  Scaling of Connectivity in Marine Populations , 2006, Science.

[45]  D. Jollivet,et al.  Population genetics and hydrodynamic modeling of larval dispersal dissociate contemporary patterns of connectivity from historical expansion into European shelf seas in the polychaete Pectinaria koreni , 2009 .

[46]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[47]  Karim Hodge,et al.  Over-water dispersal of lizards due to hurricanes , 1998, Nature.

[48]  L. Waits,et al.  Estimating the probability of identity among genotypes in natural populations: cautions and guidelines , 2001, Molecular ecology.

[49]  Paul R. Armsworth,et al.  The structure of reef fish metapopulations: modelling larval dispersal and retention patterns , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[50]  Bruce Rannala,et al.  Bayesian inference of recent migration rates using multilocus genotypes. , 2003, Genetics.

[51]  P. Sale,et al.  Metapopulation ecology in the sea: from Levins' model to marine ecology and fisheries science , 2004 .

[52]  M. Stephens,et al.  Inferring weak population structure with the assistance of sample group information , 2009, Molecular ecology resources.

[53]  I. Baums A restoration genetics guide for coral reef conservation , 2008, Molecular ecology.

[54]  T. Hughes,et al.  RECRUITMENT FAILURE, LIFE HISTORIES, AND LONG‐TERM DECLINE OF CARIBBEAN CORALS , 2000 .

[55]  A. Szmant Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa , 1991 .

[56]  D. Ayre,et al.  Climate change, genotypic diversity and gene flow in reef-building corals , 2004 .

[57]  K. Ellingsen Soft-sediment benthic biodiversity on the continental shelf in relation to environmental variability , 2002 .

[58]  A. Baird,et al.  Survival dynamics of scleractinian coral larvae and implications for dispersal , 2008, Coral Reefs.

[59]  R. Cowen,et al.  Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish , 2006, Proceedings of the Royal Society B: Biological Sciences.

[60]  K. Selkoe,et al.  Ocean currents help explain population genetic structure , 2010, Proceedings of the Royal Society B: Biological Sciences.

[61]  T. M. McGovern,et al.  MECHANISMS OF REPRODUCTIVE ISOLATION AMONG SYMPATRIC BROADCAST-SPAWNING CORALS OF THE MONTASTRAEA ANNULARIS SPECIES COMPLEX , 2004, Evolution; international journal of organic evolution.

[62]  A. Bohonak,et al.  Dispersal, Gene Flow, and Population Structure , 1999, The Quarterly Review of Biology.

[63]  Claire B. Paris,et al.  Surfing, spinning, or diving from reef to reef: effects on population connectivity , 2007 .

[64]  Paul R. Armsworth,et al.  RECRUITMENT LIMITATION, POPULATION REGULATION, AND LARVAL CONNECTIVITY IN REEF FISH METAPOPULATIONS , 2002 .

[65]  S. Palumbi POPULATION GENETICS, DEMOGRAPHIC CONNECTIVITY, AND THE DESIGN OF MARINE RESERVES , 2003 .

[66]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[67]  Claire B Paris-Limouzy,et al.  A bio‐oceanographic filter to larval dispersal in a reef‐building coral , 2006 .

[68]  S. Palumbi,et al.  Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. , 2006, The Journal of heredity.

[69]  B. Kjerfve,et al.  Magdalena river: interannual variability (1975–1995) and revised water discharge and sediment load estimates , 2000 .